Key Residues at the Riboflavin Kinase Catalytic Site of the Bifunctional Riboflavin Kinase/FMN Adenylyltransferase From Corynebacterium ammoniagenes

Cell Biochemistry and Biophysics

Volumn 65, Issue 1, 2013, Pages 57-68

  Serrano, Ana ^a   Frago, Susana ^a   Herguedas, Beatriz ^a   Martínez Júlvez, Marta ^a   Velázquez Campoy, Adrián ^a,b   Medina, Milagros ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b FUNDACIÓN ARAID   (Spain)

Author keywords

ATP:FMN adenylyltransferase; ATP:riboflavin kinase; Catalytic activity; FAD synthetase; Site directed mutagenesis; Substrate binding

Indexed keywords

CORYNEBACTERIUM; CORYNEBACTERIUM AMMONIAGENES; PROKARYOTA;

EID: 84871501565     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-012-9403-9     Document Type: Article

References (40)

1. Manstein, D. J., & Pai, E. F. (1986). Purification and characterization of FAD synthetase from Brevibacterium ammoniagenes. Journal of Biological Chemistry, 261, 16169-16173.
2. Mack, M., van Loon, A. P., & Hohmann, H. P. (1998). Regulation of riboflavin biosynthesis in Bacillus subtilis is affected by the activity of the flavokinase/flavin adenine dinucleotide synthetase encoded by ribC. Journal of Bacteriology, 180, 950-955.
3. McCormick, D. B. (1989). Two interconnected B vitamins: riboflavin and pyridoxine. Physiological Reviews, 69, 1170-1198.
4. 2) and health. American Journal of Clinical Nutrition, 77, 1352-1360.
5. Bacher, A. (1991). Biosynthesis of flavins. In F. Müller (Ed.), Chemistry and biochemistry of flavoproteins (pp. 215-259). Boca Raton, FL: CRC Press.
6. Bacher, A. (1991). Riboflavin kinase and FAD synthetase. In F. Müller (Ed.), Chemistry and biochemistry of flavoproteins (pp. 349-370). Boca Raton, FL: CRC Press.
7. Eisenreich, W., Schwarzkopf, B., & Bacher, A. (1991). Biosynthesis of nucleotides, flavins, and deazaflavins in Methanobacterium thermoautotrophicum. Journal of Biological Chemistry, 266, 9622-9631.
8. Volk, R., & Bacher, A. (1991). Biosynthesis of riboflavin. Studies on the mechanism of l-3, 4-dihydroxy-2-butanone 4-phosphate synthase. Journal of Biological Chemistry, 266, 20610-20618.
9. Efimov, I., Kuusk, V., Zhang, X., & McIntire, W. S. (1998). Proposed steady-state kinetic mechanism for Corynebacterium ammoniagenes FAD synthetase produced by Escherichia coli. Biochemistry, 37, 9716-9723.
10. Barile, M., Brizio, C., Valenti, D., De Virgilio, C., & Passarella, S. (2000). The riboflavin/FAD cycle in rat liver mitochondria. European Journal of Biochemistry, 267, 4888-4900.
11. Giancaspero, T. A., Locato, V., de Pinto, M. C., De Gara, L., & Barile, M. (2009). The occurrence of riboflavin kinase and FAD synthetase ensures FAD synthesis in tobacco mitochondria and maintenance of cellular redox status. FEBS Journal, 276, 219-231.
12. Sandoval, F. J., Zhang, Y., & Roje, S. (2008). Flavin nucleotide metabolism in plants: monofunctional enzymes synthesize FAD in plastids. Journal of Biological Chemistry, 283, 30890-30900.
13. Pallotta, M. L., Brizio, C., Fratianni, A., De Virgilio, C., Barile, M., & Passarella, S. (1998). Saccharomyces cerevisiae mitochondria can synthesise FMN and FAD from externally added riboflavin and export them to the extramitochondrial phase. FEBS Letters, 428, 245-249.
14. Mashhadi, Z., Xu, H., Grochowski, L. L., & White, R. H. (2010). Archaeal ribL: a new FAD synthetase that is air sensitive. Biochemistry, 49, 8748-8755.
15. Mashhadi, Z., Zhang, H., Xu, H., & White, R. H. (2008). Identification and characterization of an archaeon-specific riboflavin kinase. Journal of Bacteriology, 190, 2615-2618.
16. Yruela, I., Arilla-Luna, S., Medina, M., & Contreras-Moreira, B. (2010). Evolutionary divergence of chloroplasts FAD synthetase proteins. BMC Evolutionary Biology, 10, 311.
17. Torchetti, E. M., Bonomi, F., Galluccio, M., Gianazza, E., Giancaspero, T. A., Lametti, S., et al. (2011). Human FAD synthase (isoform 2): a component of the machinery that delivers FAD to apo-flavoproteins. FEBS Journal, 278, 4434-4449.
18. Torchetti, E. M., Brizio, C., Colella, M., Galluccio, M., Giancaspero, T. A., Indiveri, C., et al. (2010). Mitochondrial localization of human FAD synthetase isoform 1. Mitochondrion, 10, 263-273.
19. Wu, M., Repetto, B., Glerum, D. M., & Tzagoloff, A. (1995). Cloning and characterization of FAD1, the structural gene for flavin adenine dinucleotide synthetase of Saccharomyces cerevisiae. Molecular and Cellular Biology, 15, 264-271.
20. Santos, M. A., Jimenez, A., & Revuelta, J. L. (2000). Molecular characterization of FMN1, the structural gene for the monofunctional flavokinase of Saccharomyces cerevisiae. Journal of Biological Chemistry, 275, 28618-28624.
21. Herguedas, B., Martínez-Júlvez, M., Frago, S., Medina, M., & Hermoso, J. A. (2010). Oligomeric state in the crystal structure of modular FAD synthetase provides insights in its sequential catalysis in prokaryotes. Journal of Molecular Biology, 400, 218-230.
22. Frago, S., Velázquez-Campoy, A., & Medina, M. (2009). The puzzle of ligand binding to Corynebacterium ammoniagenes FAD synthetase. Journal of Biological Chemistry, 284, 6610-6619.
23. Frago, S., Martínez-Júlvez, M., Serrano, A., & Medina, M. (2008). Structural analysis of FAD synthetase from Corynebacterium ammoniagenes. BMC Microbiology, 8, 160.
24. Krupa, A., Sandhya, K., Srinivasan, N., & Jonnalagadda, S. (2003). A conserved domain in prokaryotic bifunctional FAD synthetases can potentially catalyze nucleotide transfer. Trends in Biochemical Sciences, 28, 9-12.
25. Huerta, C., Borek, D., Machius, M., Grishin, N. V., & Zhang, H. (2009). Structure and mechanism of a eukaryotic FMN adenylyltransferase. Journal of Molecular Biology, 389, 388-400.
26. Wang, W., Kim, R., Yokota, H., & Kim, S. H. (2005). Crystal structure of flavin binding to FAD synthetase of Thermotoga maritima. Proteins, 58, 246-248.
27. Leulliot, N., Blondeau, K., Keller, J., Ulryck, N., Quevillon-Cheruel, S., & van Tilbeurgh, H. (2010). Crystal structure of yeast FAD synthetase (Fad1) in complex with FAD. Journal of Molecular Biology, 398, 641-646.
28. Karthikeyan, S., Zhou, Q., Osterman, A. L., & Zhang, H. (2003). Ligand binding-induced conformational changes in riboflavin kinase: structural basis for the ordered mechanism. Biochemistry, 42, 12532-12538.
29. Bauer, S., Kemter, K., Bacher, A., Huber, R., Fischer, M., & Steinbacher, S. (2003). Crystal structure of Schizosaccharomyces pombe riboflavin kinase reveals a novel ATP and riboflavin-binding fold. Journal of Molecular Biology, 326, 1463-1473.
30. Herguedas, B., Martínez-Júlvez, M., Frago, S., Medina, M., & Hermoso, J. A. (2009). Crystallization and preliminary X-ray diffraction studies of FAD synthetase from Corynebacterium ammoniagenes. Acta Crystallographica, Section F: Structural Biology and Crystallization Communications, 65, 1285-1288.
31. Karthikeyan, S., Zhou, Q., Mseeh, F., Grishin, N. V., Osterman, A. L., & Zhang, H. (2003). Crystal structure of human riboflavin kinase reveals a beta barrel fold and a novel active site arch. Structure, 11, 265-273.
32. Cheek, S., Ginalski, K., Zhang, H., & Grishin, N. V. (2005). A comprehensive update of the sequence and structure classification of kinases. BMC Structural Biology, 5, 6.
33. Leskovac, V. (2003). Comprehensive enzyme kinetics. New York: Kluwer Adacemic/Plenum Publishers.
34. Kabsch, W. (2010). XDS. Acta Crystallographica. Section D, Biological Crystallography, 66, 125-132.
35. CCP4: Collaborative Computational Project, N. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallographica. Section D, Biological Crystallography, 50, 760-763.
36. Vagin, A. A., & Teplyakov, A. (1997). MOLREP: an automated program for molecular replacement. Journal of Applied Crystallography, 30, 1022-1025.
37. Murshudov, G. N., Vagin, A. A., & Dodson, E. J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallographica. Section D, Biological Crystallography, 53, 240-255.
38. Emsley, P., & Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallographica. Section D, Biological Crystallography, 60, 2126-2132.
39. Chen, V. B., Arendall, W. B., I. I. I., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., et al. (2010). MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica. Section D, Biological Crystallography, 66, 12-21.
40. Hagihara, T., Fujio, T., & Aisaka, K. (1995). Cloning of FAD synthetase gene from Corynebacterium ammoniagenes and its application to FAD and FMN production. Applied Microbiology and Biotechnology, 42, 724-729.